Evolution of compound eye morphology underlies differences in vision between closely related Drosophila species.

BACKGROUND: Insects have evolved complex visual systems and display an astonishing range of adaptations for diverse ecological niches. Species of Drosophila melanogaster subgroup exhibit extensive intra- and interspecific differences in compound eye size. These differences provide an excellent opportunity to better understand variation in insect eye structure and the impact on vision. Here we further explored the difference in eye size between D. mauritiana and its sibling species D. simulans. RESULTS: We confirmed that D. mauritiana have rapidly evolved larger eyes as a result of more and wider ommatidia than D. simulans since they recently diverged approximately 240,000 years ago. The functional impact of eye size, and specifically ommatidia size, is often only estimated based on the rigid surface morphology of the compound eye. Therefore, we used 3D synchrotron radiation tomography to measure optical parameters in 3D, predict optical capacity, and compare the modelled vision to in vivo optomotor responses. Our optical models predicted higher contrast sensitivity for D. mauritiana, which we verified by presenting sinusoidal gratings to tethered flies in a flight arena. Similarly, we confirmed the higher spatial acuity predicted for Drosophila simulans with smaller ommatidia and found evidence for higher temporal resolution. CONCLUSIONS: Our study demonstrates that even subtle differences in ommatidia size between closely related Drosophila species can impact the vision of these insects. Therefore, further comparative studies of intra- and interspecific variation in eye morphology and the consequences for vision among other Drosophila species, other dipterans and other insects are needed to better understand compound eye structure-function and how the diversification of eye size, shape, and function has helped insects to adapt to the vast range of ecological niches.

Environmental impact on visual perception modulates behavioral responses of schooling fish to looming predators.

Aggregation in social fishes has evolved to improve safety from predators. The individual interaction mechanisms that govern collective behavior are determined by the sensory systems that translate environmental information into behavior. In dynamic environments, shifts in conditions impede effective visual sensory perception in fish schools, and may induce changes in the collective response. Here, we consider whether environmental conditions that affect visual contrast modulate the collective response of schools to looming predators. By using a virtual environment to simulate four contrast levels, we tested whether the collective state of minnow fish schools was modified in response to a looming optical stimulus. Our results indicate that fish swam slower and were less polarized in lower contrast conditions. Additionally, schooling metrics known to be regulated by non-visual sensory systems tended to correlate better when contrast decreased. Over the course of the escape response, schools remained tightly formed and retained the capability of transferring social information. We propose that when visual perception is compromised, the interaction rules governing collective behavior are likely to be modified to prioritize ancillary sensory information crucial to maximizing chance of escape. Our results imply that multiple sensory systems can integrate to control collective behavior in environments with unreliable visual information.

Why flying insects gather at artificial light.

Explanations of why nocturnal insects fly erratically around fires and lamps have included theories of "lunar navigation" and "escape to the light". However, without three-dimensional flight data to test them rigorously, the cause for this odd behaviour has remained unsolved. We employed high-resolution motion capture in the laboratory and stereo-videography in the field to reconstruct the 3D kinematics of insect flights around artificial lights. Contrary to the expectation of attraction, insects do not steer directly toward the light. Instead, insects turn their dorsum toward the light, generating flight bouts perpendicular to the source. Under natural sky light, tilting the dorsum towards the brightest visual hemisphere helps maintain proper flight attitude and control. Near artificial sources, however, this highly conserved dorsal-light-response can produce continuous steering around the light and trap an insect. Our guidance model demonstrates that this dorsal tilting is sufficient to create the seemingly erratic flight paths of insects near lights and is the most plausible model for why flying insects gather at artificial lights.

Insect neurobiology: What to do with conflicting evidence?

Sensory systems gather information from the environment so the nervous system can formulate appropriate responses. But what happens when sensory information is inconsistent? A new study demonstrates how flies respond to incompatible visual evidence of their own motion.

Insect vision: Contrast perception under fluctuating light.

Natural light levels vary tremendously, both over the day and from minute to minute, creating a formidable challenge for animals that rely on vision to survive. New work in fruit flies demonstrates the neural mechanisms that produce luminance-invariant perceptions of visual contrast.

Measuring compound eye optics with microscope and microCT images.

With a great variety of shapes and sizes, compound eye morphologies give insight into visual ecology, development, and evolution, and inspire novel engineering. In contrast to our own camera-type eyes, compound eyes reveal their resolution, sensitivity, and field of view externally, provided they have spherical curvature and orthogonal ommatidia. Non-spherical compound eyes with skewed ommatidia require measuring internal structures, such as with MicroCT (µCT). Thus far, there is no efficient tool to characterize compound eye optics, from either 2D or 3D data, automatically. Here we present two open-source programs: (1) the ommatidia detecting algorithm (ODA), which measures ommatidia count and diameter in 2D images, and (2) a µCT pipeline (ODA-3D), which calculates anatomical acuity, sensitivity, and field of view across the eye by applying the ODA to 3D data. We validate these algorithms on images, images of replicas, and µCT eye scans from ants, fruit flies, moths, and a bee.

Carbon dioxide and blood-feeding shift visual cue tracking during navigation in Aedes aegypti mosquitoes.

Haematophagous mosquitoes need a blood meal to complete their reproductive cycle. To accomplish this, female mosquitoes seek vertebrate hosts, land on them and bite. As their eggs mature, they shift attention away from hosts and towards finding sites to lay eggs. We asked whether females were more tuned to visual cues when a host-related signal, carbon dioxide, was present, and further examined the effect of a blood meal, which shifts behaviour to ovipositing. Using a custom, tethered-flight arena that records wing stroke changes while displaying visual cues, we found the presence of carbon dioxide enhances visual attention towards discrete stimuli and improves contrast sensitivity for host-seeking Aedes aegypti mosquitoes. Conversely, intake of a blood meal reverses vertical bar tracking, a stimulus that non-fed females readily follow. This switch in behaviour suggests that having a blood meal modulates visual attention in mosquitoes, a phenomenon that has been described before in olfaction but not in visually driven behaviours.

Mosquito flight: Escaping attacks in dim light.

To avoid fast attackers, animals must move somewhere their pursuer cannot follow or does not expect. A new study shows that female mosquitoes of either a diurnal or a nocturnal species each exhibit a distinct escape strategy matched to the light level they experience as they hunt for blood.

Acuity and summation strategies differ in vinegar and desert fruit flies.

An animal's vision depends on terrain features that limit the amount and distribution of available light. Approximately 10,000 years ago, vinegar flies (Drosophila melanogaster) transitioned from a single plant specialist into a cosmopolitan generalist. Much earlier, desert flies (D. mojavensis) colonized the New World, specializing on rotting cactuses in southwest North America. Their desert habitats are characteristically flat, bright, and barren, implying environmental differences in light availability. Here, we demonstrate differences in eye morphology and visual motion perception under three ambient light levels. Reducing ambient light from 35 to 18 cd/m2 causes sensitivity loss in desert but not vinegar flies. However, at 3 cd/m2, desert flies sacrifice spatial and temporal acuity more severely than vinegar flies to maintain contrast sensitivity. These visual differences help vinegar flies navigate under variably lit habitats around the world and desert flies brave the harsh desert while accommodating their crepuscular lifestyle.

Insect vision: Head saccades to reset the view.

Tracking a moving scene requires you to occasionally readjust your gaze as objects slip out of sight. A new study has found how fruit flies use head-turning strategies to reset their gaze and stabilize visual images during flight.

Stabilizing responses to sideslip disturbances in Drosophila melanogaster are modulated by the density of moving elements on the ground.

Stabilizing responses to sideslip disturbances are a critical part of the flight control system in flies. While strongly mediated by mechanoreception, much of the final response results from the wide-field motion detection system associated with vision. In order to be effective, these responses must match the disturbance they are aimed to correct. To do this, flies must estimate the velocity of the disturbance, although it is not known how they accomplish this task when presented with natural images or dot fields. The recent finding, that motion parallax in dot fields can modulate stabilizing responses only if perceived below the fly, raises the question of whether other image statistics are also processed differently between eye regions. One such parameter is the density of elements moving in translational optic flow. Depending on the habitat, there might be strong differences in the density of elements providing information about self-motion above and below the fly, which in turn could act as selective pressures tuning the visual system to process this parameter on a regional basis. By presenting laterally moving dot fields of different densities we found that, in Drosophila melanogaster, the amplitude of the stabilizing response is significantly affected by the number of elements in the field of view. Flies countersteer strongly within a relatively low and narrow range of element densities. But this effect is exclusive to the ventral region of the eye, and dorsal stimuli elicit an unaltered and stereotypical response regardless of the density of elements in the flow. This highlights local specialization of the eye and suggests the lower region may play a more critical role in translational flight stabilization.

Light environment drives evolution of color vision genes in butterflies and moths.

Opsins, combined with a chromophore, are the primary light-sensing molecules in animals and are crucial for color vision. Throughout animal evolution, duplications and losses of opsin proteins are common, but it is unclear what is driving these gains and losses. Light availability is implicated, and dim environments are often associated with low opsin diversity and loss. Correlations between high opsin diversity and bright environments, however, are tenuous. To test if increased light availability is associated with opsin diversification, we examined diel niche and identified opsins using transcriptomes and genomes of 175 butterflies and moths (Lepidoptera). We found 14 independent opsin duplications associated with bright environments. Estimating their rates of evolution revealed that opsins from diurnal taxa evolve faster-at least 13 amino acids were identified with higher dN/dS rates, with a subset close enough to the chromophore to tune the opsin. These results demonstrate that high light availability increases opsin diversity and evolution rate in Lepidoptera.

Insect Neurobiology: How a Small Spot Stops a Fly.

Animals often respond to small moving features very differently than they do to large moving fields. A new study finds that viewing small spots causes walking fruit flies to stop in their tracks, and identifies the cellular pathway that processes this signal.

Ventral motion parallax enhances fruit fly steering to visual sideslip.

Flies and other insects use incoherent motion (parallax) to the front and sides to measure distances and identify obstacles during translation. Although additional depth information could be drawn from below, there is no experimental proof that they use it. The finding that blowflies encode motion disparities in their ventral visual fields suggests this may be an important region for depth information. We used a virtual flight arena to measure fruit fly responses to optic flow. The stimuli appeared below (n = 51) or above the fly (n = 44), at different speeds, with or without parallax cues. Dorsal parallax does not affect responses, and similar motion disparities in rotation have no effect anywhere in the visual field. But responses to strong ventral sideslip (206° s-1) change drastically depending on the presence or absence of parallax. Ventral parallax could help resolve ambiguities in cluttered motion fields, and enhance corrective responses to nearby objects.

Small eyes in dim light: Implications to spatio-temporal visual abilities in Drosophila melanogaster.

Fruit flies, Drosophila melanogaster, are active over a range of light intensities in the wild, but lab-reared flies are often tested only in bright light. Similarly, scarce feeding during larval stages-common in nature-generates smaller adults, and a wide range of eye sizes not found in well-fed lab colonies. Both dimmer light and smaller eyes limit light capture and have undetermined effects on visual behaviors such as flight. In this study, we used moving sinusoidal gratings to test spatial acuity, temporal acuity, and contrast threshold of female flies of varying eye sizes at different light intensities. We also investigated vision in the smaller and often neglected male fruit flies. As light intensity drops from 50.1 lx to 0.3 lx, flies have a reduced spatial acuity (females: from 0.1 to 0.06 cycles per degree, CPD, males: 0.1 to 0.04 CPD) and temporal acuity (females: from 50 Hz to 10 Hz, males: 25 Hz to 10 Hz), and an increased contrast detection threshold (females: from 10% to 29%, males: 19% to 48%). We find no major sex-specific differences after accounting for eye size. Visual abilities in both small (eye area of 0.1-0.17 mm2) and large flies (0.17-0.23 mm2) suffer at 0.3 lx compared to 50.1 lx, but small flies suffer more (spatial acuity: 0.03 vs 0.06 CPD, contrast threshold: 76% vs 57%, temporal acuity: 5 Hz vs 10 Hz). Our results suggest visual abilities of small flies suffer more than large flies at low light levels, possibly leading to size- and light intensity-dependent effects on foraging, navigation, and flight.

Insect Neurobiology: What to Make of a Small Spot?

Vertical stripes have long been known to attract laboratory fruit flies, but small spots, presumably common in the wild, seemed only to avert them. A new study finds odor can reverse this, demonstrating that flies respond to shapes more judiciously than was thought.

Fruit flies increase attention to their frontal visual field during fast forward optic flow.

Fruit flies must compensate for the limited light gathered by the tiny facets of their eyes, and image motion during flight lowers light catch even further. Motion blur is especially problematic in fast regions of the visual field, perpendicular to forward motion, but flow fields also contain slower regions, less affected by blur. To test whether fruit flies shift their attention to predictably slower regions of a flow field, we placed flies in an arena simulating forward flight and measured responses to turning cues in different visual areas. We find that during fast forward flight, fruit flies respond more strongly to turning cues presented directly in front, and less strongly to cues presented to the sides, supporting the hypothesis that flying fruit flies shift visual attention to slower moving regions less affected by motion blur.

Insect Neurobiology: Optical Illusions at the Cellular Level.

The reverse-phi illusion has been one key to understanding the use of correlation for motion perception in humans and many other animals. A new study finds the source of this illusion at the cellular level in fruit flies.

Small fruit flies sacrifice temporal acuity to maintain contrast sensitivity.

Holometabolous insects, like fruit flies, grow primarily during larval development. Scarce larval feeding is common in nature and generates smaller adults. Despite the importance of vision to flies, eye size scales proportionately with body size, and smaller eyes confer poorer vision due to smaller optics. Variable larval feeding, therefore, causes within-species differences in visual processing, which have gone largely unnoticed due to ad libitum feeding in the lab that results in generally large adults. Do smaller eyes have smaller ommatidial lenses, reducing sensitivity, or broader inter-ommatidial angles, reducing acuity? And to what extent might neural processes adapt to these optical challenges with temporal and spatial summation? To understand this in the fruit fly, we generated a distribution of body lengths (1.67-2.34 mm; n = 24) and eye lengths (0.33-0.44 mm; n = 24), resembling the distribution of wild-caught flies, by removing larvae from food during their third instar. We find smaller eyes (0.19 vs.0.07 mm2) have substantially fewer (978 vs. 540, n = 45) and smaller ommatidia (222 vs. 121 µm2;n = 45) separated by slightly wider inter-ommatidial angles (4.5 vs.5.5°; n = 34). This corresponds to a greater loss in contrast sensitivity (<50%) than spatial acuity (<20%). Using a flight arena and psychophysics paradigm, we find that smaller flies lose little spatial acuity (0.126 vs. 0.118CPD; n = 45), and recover contrast sensitivity (2.22 for both; n = 65) by sacrificing temporal acuity (26.3 vs. 10.8Hz; n = 112) at the neural level. Therefore, smaller flies sacrifice contrast sensitivity to maintain spatial acuity optically, but recover contrast sensitivity, almost completely, by sacrificing temporal acuity neurally.